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British Journal of Nutrition (1995), 73, 613423 613

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The glycaemic index of foods containing sugars: comparison of foods with naturally-occurring v. added sugars* BY JANETTE BRAND MILLER, EDNA PANG AND LOUISE BROOMHEAD Human Nutrition Unit, Department of Biochemistry, University of Sydney, NS W, Australia

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(Received 8 June 1994 - Revised 27 July 1994 - Accepted 24 August 1994)

170.106.33.19 The primary aim of the present study was to expand the glycaemic index (GI) database by determining the GI and insulin index values of thirty-nine foods containing sugars in healthy adults. The second aim was to examine the hypothesis that glycaemic and insulin responses to foods which contain added sugar(@are higher than responses to foods containing naturally-occumng sugars. Eight healthy subjects , on

drswn from a pool of eighteen consumed 50 g portions (except 25 g carbohydrate portions 27 Sep 2021 at 13:50:38 for ) of the test foods. The GI and insulin index were determined according to standardized methodology and expressed on a scale on which = 100. The median GI and insulin index values of all foods tested were 56 (range 14 to 80) and 56 (range 24 to 124) respectively. The median GI of the foods containing added sugars was similar to that of foods containing naturally-occurring sugars (58 Y. 53 respectively, P = 0.08). Likewise, the median insulin index of the foods containing added sugars was not significantly different from that of foods Containing naturally-occurring sugars (61 v. 56 respectively, P = 0.16). There was no evidence of ‘rebound hypoglycaemia’ or excessive insulin secretion relative to , subject to the Cambridge Core terms of use, available at the glucose response. We conclude that most foods containing sugars do not have a high GI. In addition, there is often no difference in responses between foods containing added sugars and those containing naturally-wcurring sugars. Glycaemic index: Plasma glucose: Insulin : Sugars : Carbohydrate

A decade ago Jenkins, Wolever and co-workers introduced the concept of glycaemic index (GI) to rank foods according to their postprandial impact on plasma glucose levels (Jenkins et af. 1981). Since then the GI values of over 200 foods have been determined (Brand et af. 1985; Jenkins el al. 1988). Many diabetes associations have accepted the principle of the GI, but they recommend that more research is needed for general application (Brand Miller, 1994). Apart from some fruits, most of the foods tested have been high in starch rather than sugars. https://www.cambridge.org/core/terms Sugars are an important component of diets in developed countries, providing about 20 % of the total energy consumed and nearly half the total carbohydrate (Glinsmann et al. 1986; Baghurst et al. 1989; Department of Health, 1989). Approximately half the sugar is derived from added sugars and the other half from naturally-occurring sources, such as and milk. The glycaemic and insulin responses to sugars are also relevant to sports performance (Thomas et af. 1991), satiety (Holt et af. 1992) and serotonin-related phenomena, such as sleepiness (Lyons & Truswell, 1988). The GI of foods containing sugars should also be considered in the emergency treatment of hypoglycaemia. The common assumption that

. foods containing sugars will produce a more rapid glycaemic response than starchy foods https://doi.org/10.1079/BJN19950063 has little scientific basis.

* No reprints will be available. Downloaded from

6 14 J. BRAND MILLER AND OTHERS The primary aim of the present study was therefore to expand the GI database by determining the GI for a wide range of common foods containing simple sugars, including https://www.cambridge.org/core sources of both refined and naturally-occurring sugars. The selection of foods was based on those that had not been tested in previous GI studies. Insulin indices were also measured to examine the hypothesis that insulin responses to foods containing sugars are inappropriately high relative to the degree of glycaemia. Lastly the data were also used to examine the hypothesis that glycaemic and insulin responses to foods which contain added sugar(s) are higher than those to foods containing naturally-occurring sugars.

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MATERIALS AND METHODS Foods Forty-two products were studied, thirty-nine of which were significant sources of simple 170.106.33.19 sugars. The majority had not been previously tested for their GI. White bread (Tip Top; George Weston Foods, Chatswood, NSW, Australia) and two unsweetened cracker-type

products (Saom and Jatz- ; Arnott's Biscuits, Homebush, NSW, Australia), which are , on

manufactured without added sugar, were also studied for comparison. The chemical 27 Sep 2021 at 13:50:38 composition of the foods was supplied by the manufacturers or determined from food tables (English & Lewis, 1991). The foods were studied in food groups (e.g. breakfast cereals, fruit, ) and the order of testing within each group was randomized. White bread was used as the reference food and tested at least once for each group of foods.

Study design , subject to the Cambridge Core terms of use, available at Each food was tested in eight subjects drawn from a pool of eighteen healthy volunteers with normal glucose tolerance. The same group of individuals tested foods within the one food group and some subjects volunteered for several food groups. Their ages ranged from 19 to 59 years (mean 28, SD 10 years) and their body mass index (BMI) from 18 to 27 kg/m2 (mean 22, SD 3 kg/m2). The subjects consumed portions of each food containing 50 g available carbohydrate except the tropical fruits (with high water content), for which 25 g carbohydrate portions were consumed. The foods were tested in random order at approximately the same time of the morning after a 10 h overnight fast. Foods were consumed evenly over 12 min. The breakfast cereals were consumed with 150 ml full-cream milk (37 g fat/l) which contributed an additional 7 g lactose. The meals were consumed with additional water so that the total meal volume was 600 ml in all cases except fruit, where the final volume was 700 ml. The tests were given about 1 week apart. Finger-prick capillary blood samples were taken at 0 min (fasting), 15, 30, 60, 90 and

120 min after the meal was commenced. Hands were placed in a 45" water bath for at least https://www.cambridge.org/core/terms 2 min before puncturing with an Autolet device (Owen Mumford Ltd, Woodstock, Oxon) using Autoclix lancets (Boehringer Mannheim, Mannheim, Germany). Blood (800 pl) was collected into 1 ml tubes with heparin, centrifuged and the plasma stored at -20" before analysis. Glucose was assayed using the glucose hexokinase (EC 2.7.1.1) method on a Cobas Fara centrifugal analyser (Roche Diagnostica, Basle, Switzerland) and insulin by radioimmunoassay with the Bio-RIA 1251-InsulinChromacode Radioimmunoassay kit (Bio-Mega Diagnostica Inc., Hamon, Montreal, Canada). The GI and insulin index of each food were calculated as described previously (Brand et al. 1985) using a 50 g carbohydrate portion of white bread as the reference food. Because

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the tropical fruits were consumed in 25 g carbohydrate portions, the incremental area https://doi.org/10.1079/BJN19950063 under the curve was doubled. This was justified on the basis of the proven linear doseresponse relationship between the area under the curve and the amount of carbohydrate consumed in the range 25 to 50 g (Jenkins et al. 198 1). The GI of every food Downloaded from

GLYCAEMIC INDEX OF FOODS CONTAINING SUGAR 615 was multiplied by the factor 70/100 in order to express the final result on a scale on which

https://www.cambridge.org/core glucose = 100 (when glucose is the reference food, the GI of white bread is 70). Jenkins et al. (1988) have made this adjustment in the opposite direction to express their early results with a white-bread standard. We believe that an index where glucose is 100 is more logical and easier to explain to patients. The Dixon test for extreme values (Dixon, 1953) was applied in a few instances to exclude very high values from calculation of the mean. For these foods the number of subjects in the group was seven. Linear regression analysis was used to test for association between glycaemic and insulin responses and between the nutrient content of the foods and their GI or insulin index. Comparisons between natural and refined sources of sugars were made . IP address: using the Mann Whitney U test because the data were not normally distributed. The protocol was approved by the Medical Ethical Review Committee of the University of Sydney and subjects gave written, informed consent. 170.106.33.19

RESULTS , on

The GI and insulin index of each food were calculated as described previously (Brand et 27 Sep 2021 at 13:50:38 al. 1985). In practice the reference food was white bread but the final result was multiplied by 70/100 in order to use a scale where glucose = 100. The final GI and insulin index values for the foods tested are shown in Table 1. The GI values ranged from 14 (SE 4) for low-fat, artificially sweetened yoghurt to 102 (SE 9) for the glucose tablets (Glucodin@).The median GI of all foods tested was 56. The insulin index values ranged from 24 (SE 8) for dried apricots to 124 (SE 21) for COCOPops@ (a sweetened, puffed rice cereal), the median insulin , subject to the Cambridge Core terms of use, available at index being 56. There was a good correlation between GI and insulin index (r 0.69, P < 0.001). The median GI of the seventeen foods containing only naturally-occurring sugars was similar to that of the twenty-one foods containing added sugars (53 v. 58 respectively, P = 0.08, Fig. 1). Similarly, the median insulin index of the foods containing naturally- occurring sugars was not significantly different from that of the foods containing added sugars (56 v. 61, P = 0.16). (Glucose tablets and the cracker biscuits made without sugar were excluded from this analysis because they contained neither naturally-occurring sugars nor significant amounts of added sucrose.) When foods were compared within categories ( products, dairy products, canned fruit, beverages), there were no significant differences for cakes, muffins and most made with or without added sugars (Fig. 2). However, there were significant differences among dairy products, canned peaches and beverages according to the presence or absence of added sugars (Fig. 3).

There was no evidence of ‘rebound hypoglycaemia’ (undershoot of the baseline plasma https://www.cambridge.org/core/terms glucose value) within 2 h of consumption of any of the foods. Fig. 4 shows that sugar in some forms of confectionery produces a response similar to that to bread with no evidence of rebound hypoglycaemia. Plasma glucose and insulin levels had returned to fasting levels withm the 2 h except in the case of bread. Correlations were calculated between GI and the fat, protein, sugar and fibre contents of the foods in order to determine whether macronutrient content of the foods influenced the GI value. A significant negative relationship was found between the protein content of the food (per 50 g carbohydrate portion) and the GI (r 0.63, P -= 0.05, n 36, Fig. 5), but this did not hold for the insulin index. There was no significant relationship between GI and fat,

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GI and sugar or GI and fibre in the foods per 50 g carbohydrate portion (Fig. 5). Similarly https://doi.org/10.1079/BJN19950063 there was no relationship between nutrient content and insulin index (results not shown). Downloaded from https://www.cambridge.org/core/terms

https://www.cambridge.org/core Table 1. The glycaemic index, insulin index and composition of the foods (glkg edible portion)

Glycaemic index Insulin index (glucose = 100) (glucose = 100) Dietary Protein Fat Carbohvdrate Sugars fibre

. Food n Mean SE Mean se https://doi.org/10.1079/BJN19950063 Breakfast cereals

COCOPops- (puffed rice with cocoa, Kellogg) 8 77 8 124 21 47 25 863 390 (r) 17 . IP address: Nutrigrain@ (extruded cereal, Kellogg) 8 66 12 73 17 21 27 715 350 (r) 15

Natural muesli (oats, fruit, nuts, Uncle Toby’s) 8 56 8 53 10 113 70 650 213 (r) 107 ~ Toasted muesli (oats, fruit, nuts, F’urina) 8 43 4 35 4 80 165 578 200 (r) 124 w

~ Sultana Brans (wheat bran flakes, Kellogg) 8 52 I 45 11 102 16 172 230 (r) 165 * 170.106.33.19 canned fruit U Peaches in natural juice (Goulburn Valley) 8 30 4 30 8 5 1 105 96 (4 14 Peaches in heavy syrup (Letona) 8 58 11 50 I 13 2 150 136 (r) 10 - Dairy products r Chocolate milk (Lite White@with sugar) 8 34 4 69 12 42 14 103 103 (r) orm , on Chocolate milk (Lite White@+ Aspartame) 8 24 6 34 7 42 15 58 58 (4 ow 27 Sep 2021 at 13:50:38 Yoghurt, low fat, with fruit and sugar (Ski@) 8 33 7 28 5 50 2 154 154 (r) 0 * Yoghurt, low fat, with fruit+Aspartame (Ski@) 7 14 4 63 9 52 2 64 64 (4 1105 Vitarim (frozen fruit confection) 8 28 6 21 5 2 1 230 229 (n) Ice-cream, low fat (Light@, Peters) 7 50 8 42 7 23 15 120 91 0.1 02 Bakery products ND Banana cake made without sugar I 55 10 53 9 ND ND 360 89 (4 s

Banana cake made with sugar 8 47 8 55 9 ND ND 480 298 (r) ND , subject to the Cambridge Core terms of use, available at Apple muffins made without sugar 8 48 10 61 18 ND ND 313 86 (n) ND Apple muffins made with sugar 8 44 6 65 10 ND ND 476 176 (r) ND Continental fruit loaf (bread with dried fruit) 8 41 6 62 14 ND ND 520 ND(n) ND Fruit Mango 7 51 3 61 12 10 2 126 121 (n) 16 Pawpaw 7 56 6 49 7 4 1 69 69 (n) 23 Rockrnelon/cantaloupe 8 65 9 19 10 5 1 47 47 (n) 10 Wa t erm e1 on 8 12 13 73 15 3 2 50 50 (4 6 Pineapple 8 66 7 56 7 10 1 80 80 (4 21 Kiwi fruit 7 58 7 62 2 14 2 98 98 (4 33 Downloaded from https://www.cambridge.org/core/terms

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. Dried fruit https://doi.org/10.1079/BJN19950063 Dried apricots 8 30 7 24 8 45 4 683 683 (n) 240 cds Sultanas 8 56 11 32 8 18 0 763 763 (n) 70 0 Biscuits (cookies) and crackers & . IP address: Milk Arrowroot@ (sweet biscuits, Arnotts) 8 69 7 69 8 66 104 80 1 217 (r) 29 5 Shredded Wheatmeal- (sweet biscuits, Amotts) 7 62 4 55 6 85 152 711 201 (r) 48 Q Highland Oatmeal@(sweet biscuits, Westons) 7 55 8 36 5 62 156 730 240 (r) 50 Morning Coffee@(sweet biscuits, Arnotts) 8 79 6 80 10 60 137 762 212 (r) 30 170.106.33.19 Sao@ (savoury cracker biscuits, Arnotts) 8 70 9 51 6 111 153 670 32 35 2 Jab@(savoury cracker biscuits, Arnotts) 8 55 5 41 5 81 200 699 50 34 x Confectionery 0 Muesli bars (Uncle Toby's) I 61 I 47 9 58 112 688 246 (r) 51 Life Savers" (peppermint candy) 8 70 6 73 11 5 I 980 980 (r) 02: , on Jelly beans (Allen's) 8 80 8 98 10 1 6 900 900 (r) 0 0 27 Sep 2021 at 13:50:38 Chocolate (milk, Cadbury's) 8 49 6 61 8 84 303 591 567 (r) 8: Concentrated sources of sugar 0 Honey (pure, Capilano) 8 58 6 58 7 5 0 830 830 (n) 00 Glucodin= (glucose tablets) 7 102 9 97 24 0 0 900 900 z Beverages OH Orange juice (unsweetened, Quekh) 8 53 6 56 8 6 0 85 80 (n) 3 2 Orange cordial (Berri) 8 66 8 69 12 0 0 80 35 80 (r) , subject to the Cambridge Core terms of use, available at Orange soft drink (Fanta") 7 68 6 84 18 0 0 134 134 (r) 02--

ND, not determined; (r), the main source of sugars is refined sugar (sucrose), but some foods will also contain naturally-occurringsugars; (n), only naturally-occurring 0 sugars are present. w9 Downloaded from https://www.cambridge.org/core/terms

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Fig. 3. Glycaemic index values for dairy products and fruits with and without added sugars. (A), comparison of chocolate milk and yoghurt made with (B) or without (0)added sugars. Mean values were significantly different for the two products, * P < 0.05, ** P < 0.01. (B), comparison of canned peaches and orange beverages made with ) and without (0)added sugars. Peaches in juice were significantly different from those in syrup, ** P < 0.01 ; orange juice was sigdicantly different from Fanta-, * P < 0.05.

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Time (min) https://doi.org/10.1079/BJN19950063 Fig. 4. Plasma glucose change after two confectionery items (Life Savers (A)and jelly beans (m)) compared with equal carbohydrate portions of white bread (---) and glucose tablets (0,Glucodin- tablets). The figure shows that sugar in the form of confectionery produces a response similar to that of bread with no evidence of rebound hypoglycaemia within 2 h of consumption. Downloaded from

620 J. BRAND MILLER AND OTHERS

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DISCUSSION This study indicates that most foods containing sugars do not have a high GI. The majority fell within the intermediate range (50-70) on the GI scale where glucose = 100. The results belie the commonly held belief that foods containing added sugars produce higher glycaemic and insulin responses than starchy foods. The GI of bread is about 70 and potatoes have a GI of 70-90 depending on the method of preparation (Jenkins et al. 1981). The majority (over 80 %) of 'sugary' foods tested in the present study had a GI lower than 70. Recently, Wolever et al. (1994) showed that the strongest determinant of whole diet GI in 340 individuals with non-insulin-dependent diabetes mellitus (NIDDM) was the intake

of simple sugars which correlated inversely with the diet GI. The present findings are https://www.cambridge.org/core/terms further evidence that foods rich in simple sugars usually have lower GI values than most common starchy foods. Simple sugars in their natural state in plant foods are thought to give rise to flatter metabolic responses than foods containing added sucrose (Department of Health, 1989). In the present study, however, the median GI of foods containing naturally-occurring sugars was not significantly different (in a statistical or biological sense) from that of foods containing added sugars. In addition, we could find no significant difference between responses to cakes, muffins and most cookies made with or without added sugars (Fig. 2). Foods where added sugars produced substantially higher values included canned peaches,

. milk, yoghurt and soft drinks. However, even in these instances the GI values of the foods https://doi.org/10.1079/BJN19950063 containing added sugars were less than that of bread. These results support the predictability of GI in the context of mixed meals (Chew et al. 1988). It is clear that addition of sucrose (which has an intermediate GI) to a low GI food will increase the final GI, while Downloaded from

GLYCAEMIC INDEX OF FOODS CONTAINING SUGAR 62 1 addition of sucrose to a high GI food will result in a lower GI meal (Brand Miller & Lobbezoo, 1994). https://www.cambridge.org/core The low mean GI of the foods studied is best explained by the composition of the individual sugars. Sucrose is a disaccharide composed of glucose and fructose so that only half the glucose-equivalents are available compared with an equal carbohydrate portion of bread or glucose. The sweetness of fruit is determined by a mixture of glucose, fructose, sucrose and other sugars, which do not affect plasma glucose levels equally. Fructose has a very small effect on the overall rate of glucose appearance (Delarue et al. 1993). None of the foods were manufactured using high-fructose maize syrup as is commonly used in North America. . IP address: Unlike many studies in this area, the findings also expand our knowledge of insulin responses after different foods. There was a good correlation between the GI of the foods and their insulin index (r 0.69). Hence the results do not support the hypothesis that foods 170.106.33.19 containing sugars give an inappropriately high insulin response relative to the degree of glycaemia. There were some exceptions to this, for example COCOPops gave a GI of 77

(SE 8), but a mean insulin index of 124 (SE 21). Individual variation in insulin index was very , on

high for this food, with one or two subjects requiring much greater insulin secretion to 27 Sep 2021 at 13:50:38 restore euglycaemia. It is also noteworthy that the yoghurt which was sweetened with Aspartame@' (a dipeptide composed of aspartic acid and phenylalanine) gave a much higher insulin response than predicted. However, this extreme disparity between glucose and insulin response did not apply to the chocolate milk sweetened with Aspartame@. We found no evidence that bread stimulates more insulin relative to oral glucose, as reported by Bornet et al. (1987) in individuals with NIDDM. The mean glycaemic response , subject to the Cambridge Core terms of use, available at to the glucose tablets was 1.48 times that to white bread, while the mean insulin response to glucose was 1.41 times that to bread. The conflicting findings may be explained by the type of subjects studied (healthy v. diabetic) or by the mode of administration of glucose, solid in the present study and dissolved in water in the other study. An insulin index of foods deserves further research because chronic hyperinsulinaemia is thought to play an important role in the development of NIDDM and hyper- triacylglycerolaemia (DeFronzo et al. 1992). Unlike glycaemic responses, insulin responses to foods are affected by the degree of insulin resistance in the individual. Ageing, obesity and genetic inheritance all influence the degree of insulin resistance (DeFronzo et al. 1992). Furthermore, the insulin requirements of individuals with insulin-dependent diabetes are presently based on carbohydrate and energy intake rather than on precise quantitative measurements of insulin responses to foods in healthy individuals. We found that the GI of tropical/exotic fruits ranged from 51 to 72, which is higher than

that obtained previously for temperate zone fruits such as apples and oranges (34 to 44, https://www.cambridge.org/core/terms where glucose = 100; Jenkins et al. 1981). There is no obvious reason why tropical fruits should have a higher GI than temperate fruits. The methodology was similar to that used by Jenkins et al. (1981), although they used 50 g rather than 25 g carbohydrate portions of fruit. Bananas, another tropical fruit, also gave a higher GI (62) than temperate fruits in the Jenkins study. One could speculate that the cell walls of tropical fruits are softer and more readily dispersed in the gastrointestinal tract than the cell walls of temperate fruits, thereby releasing sugars more quickly. The type of fibre in temperate fruit may be different to that of tropical fruit, with a higher proportion of pectins and other viscous soluble fibres. Alternatively, the pattern of individual sugars may be different in tropical and temperate

. fruits. Using published data (Southgate et al. 1978), we calculated that the average fructose https://doi.org/10.1079/BJN19950063 content was higher (39 v. 27g/kg) and the average sucrose content was lower (20 v. 40 g/kg) in eight temperate fruits compared with the six tropical fruits studied. However, total glucose-equivalents were similar (41 v. 44 g/kg respectively), suggesting that the Downloaded from

622 J. BRAND MILLER AND OTHERS glycaemic response should also be similar. However, these figures may not represent the composition of the fruit actually tested by us. Further studies directly comparing temperate https://www.cambridge.org/core and tropical fruits of known sugar composition are obviously needed to resolve the issue. Fat in foods is known to flatten the plasma glucose curve and thus high-fat foods may appear in a favourable light according to their GI. However, the fat content of the foods was not responsible for the low GI values because over three-quarters of the foods contained less than 30 g fat/kg. Moreover, there was no correlation between fat content and either GI or insulin index (Fig. 5). Protein was the only nutrient which correlated with the GI of the foods. The inverse correlation between protein content and GI could be explained by the fact that protein is an additional stimulus for insulin secretion thereby . IP address: lowering plasma glucose and the GI (Nuttall et al. 1984). We conclude that many foods containing sugar(s), whether naturally-occurring or refined, give glycaemic and insulin responses that are similar to or lower than those of many 170.106.33.19 common starchy foods in the Western diet. Although the subjects studied were normal healthy individuals, the findings are likely to apply to individuals with diabetes (Wolever

et al. 1991). Some of our comparisons, however, should be confirmed in diabetic subjects , on

before applying the findings to clinical practice. 27 Sep 2021 at 13:50:38

We gratefully acknowledge our volunteers and the financial support of the Sydney University Nutrition Research Foundation, CSR Pty Ltd and Kellogg Australia Pty Ltd.

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Southgate, D. A. T., Paul, A. A., Dean, A. C. & Christie, A. A. (1978). Free sugars in foods. Journal of Human Nutrition 32, 335347. https://www.cambridge.org/core Thomas, D. E., Brotherhood, J. R. & Brand, J. C. (1991). Carbohydrate feeding before exercise: effect of glycemic index. International Journal of Sports Medicine 12, 180-186. Wolever, T. M. S., Jenkins, D. J. A., Jenkins, A. L. & Josse, R. G. (1991). The glycemic index: methodology and clinical implications. American Journal of Clinical Nutrition 54, 84M54. Wolever, T. M.S., Nguyen, P.-M.,Chiasson, J.-L., Hunt, J. A., Josse, R. G., Palmason, C., Rodger, N. W., Ross, S. A., Ryan, E. A. & Tan, M. H. (1994). Determinants of diet glycemic index calculated retrospectively from diet records of 342 individuals with non-insulin-dependent diabetes mellitus. American Journal of Clinical Nutrition 59, 12651269.

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